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Fate of Trace Organic Compounds in Hyporheic Zone Sediments of Contrasting Organic Carbon Content and Impact on the Microbiome

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Fate of Trace Organic Compounds in Hyporheic Zone Sediments of Contrasting Organic Carbon Content and Impact on the Microbiome water Article Fate of Trace Organic Compounds in Hyporheic Zone Sediments of Contrasting Organic Carbon Content and Impact on the Microbiome Cyrus Rutere 1 , Malte Posselt 2 and Marcus A. Horn 1,3,* 1 Department of Ecological Microbiology, University of Bayreuth, 95448 Bayreuth, Germany; [email protected] 2 Department of Environmental Science, Stockholm University, SE-106 91 Stockholm, Sweden; [email protected] 3 Institute of Microbiology, Leibniz University Hannover, 30419 Hannover, Germany * Correspondence: [email protected]; Tel.: +49-511-762-17980 Received: 15 November 2020; Accepted: 14 December 2020; Published: 15 December 2020 Abstract: The organic carbon in streambed sediments drives multiple biogeochemical reactions, including the attenuation of organic micropollutants. An attenuation assay using sediment microcosms differing in the initial total organic carbon (TOC) revealed higher microbiome and sorption associated removal efficiencies of trace organic compounds (TrOCs) in the high-TOC compared to the low-TOC sediments. Overall, the combined microbial and sorption associated removal efficiencies of the micropollutants were generally higher than by sorption alone for all compounds tested except propranolol whose removal efficiency was similar via both mechanisms. Quantitative real-time PCR and time-resolved 16S rRNA gene amplicon sequencing revealed that higher bacterial abundance and diversity in the high-TOC sediments correlated with higher microbial removal efficiencies of most TrOCs. The bacterial community in the high-TOC sediment samples remained relatively stable against the stressor effects of TrOC amendment compared to the low-TOC sediment community that was characterized by a decline in the relative abundance of most phyla except Proteobacteria. Bacterial genera that were significantly more abundant in amended relative to unamended sediment samples and thus associated with biodegradation of the TrOCs included Xanthobacter, Hyphomicrobium, Novosphingobium, Reyranella and Terrimonas. The collective results indicated that the TOC content influences the microbial community dynamics and associated biotransformation of TrOCs as well as the sorption potential of the hyporheic zone sediments. Keywords: total organic carbon; trace organic compounds; hyporheic zone; sediments; amplicon sequencing; microbial diversity 1. Introduction Wastewater-derived trace organic compounds (TrOCs) such as pharmaceuticals and personal care products are frequently detected in receiving rivers due to inefficient removal by most 1 conventional treatment processes [1,2]. Despite occurring in trace concentration ranges (ng to µg L− ), their persistence and accumulation are of ecotoxicological concern [3]. However, attenuation of such compounds via microbial transformation and sorption processes has been reported in the hyporheic zone, the saturated sediment directly beneath and lateral to the stream [2,4–6]. Both attenuation processes are significantly influenced by the organic matter content in the sediment since organic carbon fuels multiple TrOC-coupled biogeochemical reactions [7] as well as being the main sorbent for organic chemicals [8]. Water 2020, 12, 3518; doi:10.3390/w12123518 www.mdpi.com/journal/water Water 2020, 12, 3518 2 of 22 In impacted rivers and streams, most of the organic carbon derived from wastewater effluents, decomposing leaf litter and macrophytes is deposited onto the streambed sediment [9,10]. The upper section of the sediment or benthic zone as the primary contact point of such deposits has a higher concentration of organic carbon compared to subjacent layers [6,7]. Subsequently, most streambed sediments of receiving rivers are characterized by gradients in the organic carbon content along the depth profile. This bioavailable total organic carbon (TOC) is considered a major limiting factor for microbial metabolism [11]. As bacteria dominate microbial communities in streambed sediments [12–16], bacterial populations, turnover and metabolism are virtually higher in the surface sediment layer with corresponding mineralization rates decreasing exponentially with depth [6,17–19]. Additionally, as the main sorbent for organic chemicals, the decline in TOC content with increasing depth corresponds to reduced TrOC sorption potential of the sediment [16]. As rivers continue to be impacted by a wide range of emerging TrOCs, the influence of the hyporheic zone sediment TOC content on their removal becomes increasingly important. We hypothesized that hyporheic zone sediments differing in the TOC content along the depth profile host distinct microbiomes and exhibit variable TrOC removal capacities. We investigated the removal efficiency of a set of 13 TrOCs routinely discharged by a wastewater treatment plant (WWTP) using impacted hyporheic zone sediments differing in the initial TOC content. The compounds included pharmaceuticals from various pharmacological classes including nonsteroidal anti-inflammatory drugs (NSAIDs; diclofenac, ibuprofen, ketoprofen and naproxen), beta-blockers (metoprolol, propranolol), cholesterol-lowering agents (bezafibrate, clofibric acid), antihypertensive drugs (furosemide, hydrochlorothiazide), anticonvulsant (carbamazepine), an artificial sweetener (acesulfame), and a corrosion inhibitor (benzotriazole). Our objectives were to (i) determine TrOC removal efficiencies in hyporheic zone sediments differing in initial TOC concentrations via microbial transformation and sorption mechanisms, (ii) assess the response of the indigenous bacterial communities in the sediments differing in TOC concentrations to TrOC amendment, and (iii) hence identify potential bacterial TrOC degraders. To address our aims, we (i) performed a TrOC attenuation assay in biotic and abiotic batch microcosms, and (ii) characterized the response of the indigenous bacterial community using time-resolved high-throughput sequencing of the 16S rRNA genes and 16S rRNA. 2. Materials and Methods 2.1. Study Site and Sampling Sediment samples were collected from a section of the River Erpe, an urban lowland stream in Berlin, Germany, located approximately 0.7 km downstream of the Muenchehofe WWTP effluent outlet. The stream receives 60–80% of its discharge as effluents [20]. In June 2016, the site was selected for a comprehensive study on the fate of TrOCs in the hyporheic zone. The sediments at the sampling site were densely covered by macrophytes, hence minimizing light exposure onto the surface sediment [20]. Preliminary analysis of the nutrient species across the sediment profile indicated the upper 30 cm was oxic [6]. The sediment was also virtually homogenous up to about 35 cm depth and consisted mainly of sand (>50%), silt and gravel [21]. The sediment TOC concentration decreased with increasing depth. The upper layer (0–10 cm), hereafter referred to as the surface layer, and the subjacent layer (>10 cm of depth), hereafter referred to as the subsurface layer, contained 8.7% and 3.2% TOC, respectively [5], which was in a typical range of TOC found in temperate streambed environments (2.0–33%; average: 8.5%; [22]). Three sediment cores up to the 20 cm sediment depth were collected using 6 cm-diameter sediment corers (Uwitec, Mondsee, Austria). Grab samples of the surface water were also collected at the same location as the sediment cores and stored in sealed bottles. The core samples were then transferred to the laboratory and sectioned in 10 cm intervals. Sediment samples between depths 0–10 cm and 10–20 cm from the three replicate cores were manually homogenized in sterile plastic containers using alcohol-sterilized spatulas and processed aerobically under standard Water 2020, 12, 3518 3 of 22 sterile lab conditions. A portion (t0 samples) from each sectioned depth was stored at 80 C for − ◦ subsequent extraction of nucleic acids. 2.2. Chemicals and Standards Native and isotope-substituted internal standards of the test compounds—diclofenac, ibuprofen, ketoprofen, naproxen, metoprolol, propranolol, bezafibrate, clofibric acid, furosemide, hydrochlorothiazide, carbamazepine, benzotriazole and acesulfame—were purchased from Toronto Research Chemicals Inc., (North York, ON, Canada). Liquid chromatography–mass spectrometry (LC-MS) grade methanol was purchased from Merck (Darmstadt, Germany), analytical grade acetic acid ( 99.7%) from Sigma-Aldrich (Darmstadt, Germany) and LC-MS grade water was generated with ≥ a Milli-Q water purification system (Merck, Darmstadt, Germany). Stock and working solutions were prepared as reported in [4]. 2.3. Microcosm Setup Three sets of microcosms per sediment layer using duplicate samples for each of the three sediment cores were set up in 5 mL glass bottles, each containing 2 g of wet sediment and 2 mL of river water. In total, nine microcosms were set up per sediment layer (3 sediments from three × 1 cores 3). In two of the three sets, the river water was amended with approximately 500 µg L− of each of the 13 test compounds. All 13 test TrOCs occur at the sampling site, and TrOCs typically 1 range from 0.1 to 200 µg L− in surface and hyporheic pore waters [4]. TrOC concentrations applied in our microcosms were higher but in the same order of magnitude of concentrations observed in situ [4]. Such high concentrations were used to allow for an enrichment of potential TrOC degraders as previously demonstrated [23,24]. To account for sorption, one of the setups was treated with 0.1% sodium azide to reduce bacterial activity. The third set of microcosms served as an unamended biotic control and was incubated
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